Exposure to heat stress leads to striking clone-specific nymph deformity in pea aphid.

Climatic changes, such as heatwaves, pose unprecedented challenges for insects, as escalated temperatures above the thermal optimum alter insect reproductive strategies and energy metabolism. While thermal stress responses have been reported in different insect species, thermo-induced developmental abnormalities in phloem-feeding pests are largely unknown. In this laboratory study, we raised two groups of first instar nymphs belonging to two clones of the pea aphid Acyrthosiphon pisum, on fava beans Vicia faba. The instars developed and then asexually reproduced under constant exposure to a sub-lethal heatwave (27°C) for 14 days. Most mothers survived but their progenies showed abnormalities, as stillbirths and appendageless or weak nymphs with folded appendages were delivered. Clone N116 produced more deceased and appendageless embryos, contrary to N127, which produced fewer dead and more malformed premature embryos. Interestingly, the expression of the HSP70 and HSP83 genes differed in mothers between the clones. Moreover, noticeable changes in metabolism, e.g., lipids, were also detected and that differed in response to stress. Deformed offspring production after heat exposure may be due to heat injury and differential HSP gene expression, but may also be indicative of a conflict between maternal and offspring fitness. Reproductive altruism might have occurred to ensure some of the genetically identical daughters survive. This is because maintaining homeostasis and complete embryogenesis could not be simultaneously fulfilled due to the high costs of stress. Our findings shine new light on pea aphid responses to heatwaves and merit further examination across different lineages and species.

Symbiont-conferred immunity interacts with effects of parasitoid genotype and intraguild predation to affect aphid immunity in a clone-specific fashion.

BACKGROUND: Host-parasite interactions represent complex co-evolving systems in which genetic and associated phenotypic variation within a species can significantly affect selective pressures on traits, such as host immunity, in the other. While often modelled as a two-species interaction between host and parasite, some systems are more complex due to effects of host enemies, intraguild predation, and endosymbionts, all of which affect host immunity. However, it remains unclear how these factors, combined with genetic variation in the host and the parasitoid, affect host immunity. We address this question in an important agricultural pest system, the pea aphid Acyrthosiphon pisum, which shows significant intraspecific variability in immunity to the parasitoid wasp Aphidius ervi. In a complex experiment, we use a quantitative genetic design in the parasitoid, two ecologically different aphid lineages and the aphid lion Chrysoperla carnea as an intraguild predator to unravel the complex interdependencies. RESULTS: We demonstrate that aphid immunity as a key trait of this complex host-parasite system is affected by intraspecific genetic variation in the parasitoid and the aphid, the interaction of intraspecific genetic variation with intraguild predation, and differences in defensive endosymbionts between aphid lineages. Further, aphid lineages differ in their altruistic behaviour whereby infested aphids move away from the clonal colony to facilitate predation. CONCLUSIONS: Our findings provide new insights into the influence of endosymbiosis and genetic variability in an important host-parasitoid system which is influenced by natural enemies of the parasitoid and the aphid, including its endosymbiont communities. We show that endosymbiosis can mediate or influence the evolutionary arms race between aphids and their natural enemies. The outcome of these complex interactions between species has significant implications for understanding the evolution of multitrophic systems, including eco-agricultural settings.

Indirect ecological effects interact with community genetic effects in a host-parasite system and dramatically reduce parasite burden.

Community genetic (CG) effects and ecological factors create a complex set of interactions that are key drivers of evolutionary dynamics in ecological systems. To date, most studies investigating trait variation have focused on either effects of intraspecific genetic variation or on genotype by environment (GxE) interactions in isolation. Poorly investigated but very important are the interactions between CGs and indirect ecological effects (IEEs) that are caused by plant-soil interactions. Here, we tested how CGs in a cabbage host and its aphid parasite depended on the ecological conditions under which the host was grown. We established microcosms of different cabbage cultivars and aphid genotypes on soils inoculated with samples of other soils previously trained with onion. We hypothesized that such IEEs will have significantly different outcomes for ecosystems than predicted from simpler CG or GxE studies. Our analysis demonstrated a large IEE that differed by context and aphid genotype causing reduced parasite population sizes by up to 90%. The IEE is induced by insect-repellent properties and the microbiome of the onion. Our results highlight the importance of interacting IEEs and CGs for ecosystems dynamics showing that IEEs offer sustainable solutions by dramatically reducing parasite burden on cash crops.

Novel resilience in response to revitalisation after exposure to lethal salinity causes differential reproductive success in an extremely plastic organism.

Phenotypic plasticity is central to an organism's ability to adapt to variable environmental conditions. For aquatic organisms, exposure to elevated salt levels poses a challenge and organisms may fail to tolerate or survive much higher levels short-term. Here we demonstrate, for the first time, in a laboratory study of Daphnia magna that exposure to levels of salinity higher than those previously shown to lead to apparent death (paralysis) can be reversed following a transfer to optimal conditions. We established experimental populations from one clone of D. magna, each with five replicates, that were exposed to different short periods of three different lethal levels of salinity (12.27 PSU [45, 60, 90 and 120 min], 18.24 PSU [45, 60 and 90 min] and 24.22 PSU [45, 60 and 90 min]). In all populations, all individuals were paralysed at the end of their exposure, usually classified in the literature as dead. Subsequently, all individuals were transferred to optimal conditions. However, after the transfer, a proportion of the individuals not only came back from the verge of death (i.e. were revitalised), but also showed afterwards differential reproductive success over a period of 20 days, depending on the level and the length of exposure before revitalisation. Both exposure level and time had an overall negative effect on population size that differed across all treatments. Revitalisation occurred within an hour after the transfer to optimal conditions for 18.24 PSU but took 14-16 h for 12.27 PSU. There was no instantaneous revitalisation nor was there any revitalisation after 16 h no matter how long the paralysed Daphnia individuals were left in the optimal conditions. Our findings cast new light on resilience in cladocerans and suggest that abrupt environmental change can reveal novel plastic responses to extreme conditions.

Fear of predation alters clone-specific performance in phloem-feeding prey.

Fear of predation has been shown to affect prey fitness and behaviour, however, to date little is known about the underlying genetics of responses to predator-associated risk. In an effort to fill this gap we exposed four naïve clones of green peach aphid (Myzus persicae), maintained on the model crop Brassica oleracea, to different types of cues from aphid lion (Chrysoperla carnea). The respective predation risks, we termed Fear Factors, were either lethal (consumption by predator), or non-lethal (non-consumptive predator-associated cues: plant-tethered predator cadavers and homogenised shoot-sprayed or soil-infused blends of predator remains). Our results show that the non-lethal risk cues differentially impeded prey reproductive success that varied by clone, suggesting genotype-specific response to fear of predation. Furthermore, whether plants were perceived as being safe or risky influenced prey responses as avoidance behaviour in prey depended on clone type. Our findings highlight that intra-specific genetic variation underlies prey responses to consumptive and non-consumptive effects of predation. This allows selection to act on anti-predator responses to fear of predation that may ramify and influence higher trophic levels in model agroecosystems.

Parasitoid wasps influence where aphids die via an interspecific indirect genetic effect.

Host-parasite interactions are a key paradigm for understanding the process of coevolution. Central to coevolution is how genetic variation in interacting species allows parasites to evolve manipulative strategies. However, genetic variation in the parasite may also be associated with host phenotype changes, thereby changing the selection on both species. For instance, parasites often induce changes in the behaviour of their host to maximize their own fitness, yet the quantitative genetic basis for behavioural manipulation has not been fully demonstrated. Here, we show that the genotype of the parasitoid wasp Aphidius ervi has a significant effect on where its aphid host Acyrthosiphon pisum moves to die following parasitism, including the likelihood that the aphid abandons the plant. These results provide a clear example of an interspecific indirect genetic effect whereby the genetics of one species influences the expression of a specific behavioural trait in another.

Genetic effects of tank-forming bromeliads on the associated invertebrate community in a tropical forest ecosystem.

Within the area of community genetics there is an expanding volume of literature demonstrating how within-species genetic variation in temperate trees can have important effects on structuring animal and plant communities. The influence of intraspecific genetic variation on associated communities in relatively more complex ecosystems is only starting to be appreciated. Within tropical forests, epiphytic bromeliad plants often grow high in the canopy and create unique nutrient-rich microhabitats on which many invertebrate and vertebrate species depend. We investigated the influence of within-species genetic variation in the bromeliad Aechmea bracteata on the invertebrate microhabitat community. We found that more genetically similar bromeliad plants were host to more similar communities of juvenile-stage invertebrates, but not adult invertebrates. We discuss possible mechanisms for this, including differential survival and active female oviposition choice. Our work shows that the impact of within-species genetic variation on associated ecological communities may be more general than previously considered. These results agree with recent research suggesting that within-species genetic variation may perform a supporting ecosystem service for maintaining community and ecological processes.